School of BioSciences - Research Publications

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    Fine-scale mapping of physicochemical and microbial landscapes of the coral skeleton
    Ricci, F ; Tandon, K ; Mosshammer, M ; Cho, EH-J ; Blackall, LL ; Kuhl, M ; Verbruggen, H (WILEY, 2023-08)
    The coral skeleton harbours a diverse community of bacteria and microeukaryotes exposed to light, O2 and pH gradients, but how such physicochemical gradients affect the coral skeleton microbiome remains unclear. In this study, we employed chemical imaging of O2 and pH, hyperspectral reflectance imaging and spatially resolved taxonomic and inferred functional microbiome characterization to explore links between the skeleton microenvironment and microbiome in the reef-building corals Porites lutea and Paragoniastrea benhami. The physicochemical environment was more stable in the deep skeleton, and the diversity and evenness of the bacterial community increased with skeletal depth, suggesting that the microbiome was stratified along the physicochemical gradients. The bulk of the coral skeleton was in a low O2 habitat, whereas pH varied from pH 6-9 with depth. Physicochemical gradients of O2 and pH of the coral skeleton explained the β-diversity of the bacterial communities, and skeletal layers that showed O2 peaks had a higher relative abundance of endolithic algae, reflecting a link between the abiotic environment and the microbiome composition. Our study links the physicochemical, microbial and functional landscapes of the coral skeleton and provides new insights into the involvement of skeletal microbes in the coral holobiont metabolism.
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    Every refuge has its price: Ostreobium as a model for understanding how algae can live in rock and stay in business
    Tandon, K ; Pasella, MM ; Iha, C ; Ricci, F ; Hu, J ; O'Kelly, CJ ; Medina, M ; Kuehl, M ; Verbruggen, H (Elsevier, 2023-01-30)
    Ostreobium is a siphonous green alga in the Bryopsidales (Chlorophyta) that burrows into calcium carbonate (CaCO3) substrates. In this habitat, it lives under environmental conditions unusual for an alga (i.e., low light and low oxygen) and it is a major agent of carbonate reef bioerosion. In coral skeletons, Ostreobium can form conspicuous green bands recognizable by the naked eye and it is thought to contribute to the coral's nutritional needs. With coral reefs in global decline, there is a renewed focus on understanding Ostreobium biology and its roles in the coral holobiont. This review summarizes knowledge on Ostreobium's morphological structure, biodiversity and evolution, photosynthesis, mechanism of bioerosion and its role as a member of the coral holobiont. We discuss the resources available to study Ostreobium biology, lay out some of the uncharted territories in Ostreobium biology and offer perspectives for future research.
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    The Bacterial Microbiome of the Coral Skeleton Algal Symbiont Ostreobium Shows Preferential Associations and Signatures of Phylosymbiosis
    Pushpakumara, BLDU ; Tandon, K ; Willis, A ; Verbruggen, H (SPRINGER, 2023-10)
    Ostreobium, the major algal symbiont of the coral skeleton, remains understudied despite extensive research on the coral holobiont. The enclosed nature of the coral skeleton might reduce the dispersal and exposure of residing bacteria to the outside environment, allowing stronger associations with the algae. Here, we describe the bacterial communities associated with cultured strains of 5 Ostreobium clades using 16S rRNA sequencing. We shed light on their likely physical associations by comparative analysis of three datasets generated to capture (1) all algae associated bacteria, (2) enriched tightly attached and potential intracellular bacteria, and (3) bacteria in spent media. Our data showed that while some bacteria may be loosely attached, some tend to be tightly attached or potentially intracellular. Although colonised with diverse bacteria, Ostreobium preferentially associated with 34 bacterial taxa revealing a core microbiome. These bacteria include known nitrogen cyclers, polysaccharide degraders, sulphate reducers, antimicrobial compound producers, methylotrophs, and vitamin B12 producers. By analysing co-occurrence networks of 16S rRNA datasets from Porites lutea and Paragoniastrea australensis skeleton samples, we show that the Ostreobium-bacterial associations present in the cultures are likely to also occur in their natural environment. Finally, our data show significant congruence between the Ostreobium phylogeny and the community composition of its tightly associated microbiome, largely due to the phylosymbiotic signal originating from the core bacterial taxa. This study offers insight into the Ostreobium microbiome and reveals preferential associations that warrant further testing from functional and evolutionary perspectives.
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    Unravelling microalgal-bacterial interactions in aquatic ecosystems through 16S rRNA gene-based co-occurrence networks
    Pushpakumara, BLDU ; Tandon, K ; Willis, A ; Verbruggen, H (NATURE PORTFOLIO, 2023-02-16)
    Interactions between microalgae and bacteria can directly influence the global biogeochemical cycles but the majority of such interactions remain unknown. 16S rRNA gene-based co-occurrence networks have potential to help identify microalgal-bacterial interactions. Here, we used data from 10 Earth microbiome projects to identify potential microalgal-bacterial associations in aquatic ecosystems. A high degree of clustering was observed in microalgal-bacterial modules, indicating densely connected neighbourhoods. Proteobacteria and Bacteroidetes predominantly co-occurred with microalgae and represented hubs of most modules. Our results also indicated that species-specificity may be a global characteristic of microalgal associated microbiomes. Several previously known associations were recovered from our network modules, validating that biologically meaningful results can be inferred using this approach. A range of previously unknown associations were recognised such as co-occurrences of Bacillariophyta with uncultured Planctomycetes OM190 and Deltaproteobacteria order NB1-j. Planctomycetes and Verrucomicrobia were identified as key associates of microalgae due to their frequent co-occurrences with several microalgal taxa. Despite no clear taxonomic pattern, bacterial associates appeared functionally similar across different environments. To summarise, we demonstrated the potential of 16S rRNA gene-based co-occurrence networks as a hypothesis-generating framework to guide more focused research on microalgal-bacterial associations.
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    Genomic view of the diversity and functional role of archaea and bacteria in the skeleton of the reef-building corals Porites lutea and Isopora palifera
    Tandon, K ; Ricci, F ; Costa, J ; Medina, M ; Kuhl, M ; Blackall, LL ; Verbruggen, H (OXFORD UNIV PRESS, 2023-01-23)
    At present, our knowledge on the compartmentalization of coral holobiont microbiomes is highly skewed toward the millimeter-thin coral tissue, leaving the diverse coral skeleton microbiome underexplored. Here, we present a genome-centric view of the skeleton of the reef-building corals Porites lutea and Isopora palifera, through a compendium of ∼400 high-quality bacterial and archaeal metagenome-assembled genomes (MAGs), spanning 34 phyla and 57 classes. Skeletal microbiomes harbored a diverse array of stress response genes, including dimethylsulfoniopropionate synthesis (dsyB) and metabolism (DMSP lyase). Furthermore, skeletal MAGs encoded an average of 22 ± 15 genes in P. lutea and 28 ± 23 in I. palifera with eukaryotic-like motifs thought to be involved in maintaining host association. We provide comprehensive insights into the putative functional role of the skeletal microbiome on key metabolic processes such as nitrogen fixation, dissimilatory and assimilatory nitrate, and sulfate reduction. Our study provides critical genomic resources for a better understanding of the coral skeletal microbiome and its role in holobiont functioning.
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    Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses
    Ricci, F ; Tandon, K ; Black, JR ; Cao, K-AL ; Blackall, LL ; Verbruggen, H ; Raina, J-B (AMER SOC MICROBIOLOGY, 2022-04-26)
    The success of tropical scleractinian corals depends on their ability to establish symbioses with microbial partners. Host phylogeny and traits are known to shape the coral microbiome, but to what extent they affect its composition remains unclear. Here, by using 12 coral species representing the complex and robust clades, we explored the influence of host phylogeny, skeletal architecture, and reproductive mode on the microbiome composition, and further investigated the structure of the tissue and skeleton bacterial communities. Our results show that host phylogeny and traits explained 14% of the tissue and 13% of the skeletal microbiome composition, providing evidence that these predictors contributed to shaping the holobiont in terms of presence and relative abundance of bacterial symbionts. Based on our data, we conclude that host phylogeny affects the presence of specific microbial lineages, reproductive mode predictably influences the microbiome composition, and skeletal architecture works like a filter that affects bacterial relative abundance. We show that the β-diversity of coral tissue and skeleton microbiomes differed, but we found that a large overlapping fraction of bacterial sequences were recovered from both anatomical compartments, supporting the hypothesis that the skeleton can function as a microbial reservoir. Additionally, our analysis of the microbiome structure shows that 99.6% of tissue and 99.7% of skeletal amplicon sequence variants (ASVs) were not consistently present in at least 30% of the samples, suggesting that the coral tissue and skeleton are dominated by rare bacteria. Together, these results provide novel insights into the processes driving coral-bacterial symbioses, along with an improved understanding of the scleractinian microbiome.